Can sublethal parasitism destabilize predator-prey population dynamics? A model of snowshoe hares, predators and parasites

Journal of Animal Ecology

Volumn 66, Issue 2, 1997, Pages 265-278

  Ives, Anthony R ^a   Murray, Dennis L ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF IDAHO   (United States)

Author keywords

nematode; parasite host dynamics; parasite induced effects; population cycles

Indexed keywords

PARASITISM; POPULATION CYCLE; POPULATION DYNAMICS; PREDATOR-PREY INTERACTION; SNOWSHOE HARE;

LEPUS AMERICANUS; NEMATODA;

EID: 0030618148     PISSN: 00218790     EISSN: None     Source Type: Journal    
DOI: 10.2307/6027     Document Type: Article

References (82)

1. Adamcik, R.S. & Keith, L.B. (1978) Regional movements and mortality of great horned owls in relation to snowshoe hare fluctuations. Canadian Field Naturalist, 92, 228-234.
2. Adamcik, R.S., Todd, A.W. & Keith, L.B. (1978) Demographic and dietary responses of great horned owls during a snowshoe hare cycle. Canadian Field Naturalist, 92, 156-166.
3. Anderson, R.M. (1980) The dynamics and control of direct life cycle helminth parasites. Lecture Notes in Biomathematics, 39, 278-322.
4. Anderson, R.M. (1981) Infectious disease agents and cyclic fluctuations in host abundance. The Mathematical Theory of the Dynamics of Biological Populations II (eds R. W. Hiorns & D. Cooke), pp. 47-80. Academic Press, London.
5. Anderson, R.M. & May, R.M. (1978) Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology, 47, 219-249.
6. Anderson, R.M., Jackson, H.C., May, R.M. & Smith, A.M. (1981) Population dynamics of fox rabies in Europe. Nature, 289, 765-771.
7. Archibald, H.L. (1977) Is the 10-year wildlife cycle induced by a lunar cycle? Wildlife Society Bulletin, 5, 126-129.
8. Arditi, R. (1979) Relation of the Canada lynx, Lynx canadensis, cycle to a combination of weather variables. A stepwise multiple regression analysis. Oecologia, 41, 219-234.
9. Berryman, A.A. (1991) Stabilization or regulation: what it all means! Oecologia, 86, 140-143.
10. Bloomer, S.E.M., Willebrand, T., Keith, I.M. & Keith, L.B. (1995) Impact of helminth parasitism on a snowshoe hare-population in central Wisconsin: a field experiment. Canadian Journal of Zoology, 73, 1891-1898.
11. Boughton, R.V. (1932) The influence of helminth parasitism on the abundance of the snowshoe rabbit in western Canada. Canadian Journal of Research, 7, 524-547.
12. Boutin, S. (1995) Testing predator-prey theory by studying fluctuating populations of small mammals. Wildlife Research. 22, 89-100.
13. Boutin, S. Krebs, C.J., Sinclair, A.R.E. & Smith, J.N.M. (1986) Proximate causes of losses in a snowshoe hare population. Canadian Journal of Zoology, 64, 606-610.
14. Brand, C.J. & Keith, L.B. (1979) Lynx demography during a snowshoe hare decline in Alberta. Journal of Wildlife Management, 43, 827-849.
15. Brand, C.J., Keith, L.B. & Fischer, C.A. (1976) Lynx responses to changing snowshoe hare densities in central Alberta. Journal of Wildlife Management, 40, 416-428.
16. Cary, J.R. & Keith, L.B. (1979) Reproductive change in the 10-year cycle of snowshoe hares. Canadian Journal of Zoology, 57, 375-390.
17. Caswell, H. (1972) A simulation study of a time lag population model. Journal of Theoretical Biology, 34, 419-439.
18. Croll, N.A., Anderson, R.M., Gyorkos, T.W. & Ghadirian, E. (1982) The population biology and control of Ascaris lumbricoides in a rural community in Iran. Transactions of the Royal Society of Tropical Medicine and Hygiene, 76, 187-197.
19. Dobson, A.P. & Hudson, P.J. (1992) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. II. Population models. Journal of Animal Ecology, 61, 487-498.
20. Dobson, A.P., Hudson, P.J. & Lyles, A.M. (1992) Macroparasites: worms and others. Natural Enemies (ed. M. J. Crawley), pp. 329-348, Blackwell Scientific Publications, Oxford.
21. Dunsmore, J.D. (1981) The role of parasites in population regulation of the European rabbit (Oryctolagus cuniculus) in Australia. Proceedings to the Worldwide Furbearer Conference, Frostburg, Md (1980) (eds J. A. Chapman & D. Pursely), pp. 654-669. Worldwide Furbearer Conference, Inc.
22. Erickson, A.B. (1944) Helminth infections in relation to population fluctuations in snowshoe hares. Journal of Wildlife Management, 8, 134-153.
23. Finerty, J.P. (1980) The Population Ecology of Cycles in Small Mammals. Yale University Press, New Haven.
24. Fox, J.F. & Bryant, J.P. (1984) Instability of the snowshoe hare and woody plant interaction. Oecologia, 63, 128-135.
25. Gilpin, M.E. (1974) A model of the predator-prey relationship. Theoretical Population Biology, 5, 333-344.
26. Gregory, R.D. & Keymer, A.E. (1989) The ecology of host-parasite interactions. Scientific Progress, 73, 67-80.
27. Gulland, F.M.D. (1992) The role of nematode parasites in Soay sheep (Ovis aries, L.) mortality during a population crash. Parasitology, 105, 493-503.
28. Hik, D. (1995) Does risk of predation influence population dynamics? Evidence from the cyclic decline of snowshoe hares. Wildlife Research, 22, 115-129.
29. Holling, C.S. (1959) Some characteristics of simple types of predation and parasitism. Canadian Entomologist, 91, 385-398.
30. Holmes, J.C. (1982) Impact of infectious disease agents on the population growth and geographical distribution of animals. Population Biology of Infectious Diseases (eds R. M. Anderson & R. M. May), pp. 37-51. Springer-Verlag, New York.
31. Hudson, P.J. (1986) The effect of a parasitic nematode on the breeding production of red grouse. Journal of Animal Ecology, 55, 85-92.
32. Hudson, P.J., Dobson, A.P. & Newborn, D. (1985) Cyclic and non-cyclic populations of red grouse: a role for parasitism? Ecology and Genetics of Host-Parasite Interactions (eds D. Rollinson & R. M. Anderson), pp. 77-89. Academic Press, London.
33. Hudson, P.J., Dobson, A.P & Newborn, D. (1992a) Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology, 61, 681-692.
34. Hudson, P.J, Newborn, D. & Dobson, A.P. (1992b) Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. I. Monitoring and parasite reduction experiments. Journal of Animal Ecology, 61, 477-486.
35. Iversen, J.O., Spalatin, J., Fraser, C.E.O., Hanson, R.P. & Berman, D.T. (1970) The susceptibility of muskrats and snowshoe hares to experimental infection with a chlamydial agent. Canadian Journal of Comparative Medicine, 34, 80-89.
36. Ives, A.R. & May, R.M. (1985) Competition within and between species in a patchy environment: relations between microscopic and macroscopic models. Journal of Theoretical Biology, 115, 65-92.
37. Jasic, P.M. Jiminez, J.E., Castro, S.A. & Feinsinger, P. (1992) Numerical and functional response of predators to a long-term decline in mammalian prey at a semi-arid Neotropical site. Oecologia, 89, 90-101.
38. Keith, I.M., Keith, L.B. & Cary, J.R. (1986) Parasitism in a declining population of snowshoe hares. Journal of Wildlife Diseases, 22, 349-363.
39. Keith, L.B. (1963) Wildlife's Ten-year Cycle. University of Wisconsin Press, Madison.
40. Keith, L.B. (1990) Dynamics of snowshoe hare populations. Current Mammalogy (ed. H. H. Genoways), pp. 119-195. Plenum Press, New York, NY.
41. Keith, L.B. Cary, J.R., Rongstad, O.J. & Brittingham, M.C. (1984) Demography and ecology of a declining snowshoe hare population. Wildlife Monographs, 90, 1-43.
42. Keith, L.B., Cary, J.R., Yuill, T.M. & Keith, I.M. (1985) Prevalence of helminths in a cyclic snowshoe hare population. Journal of Wildlife Diseases, 21, 233-253.
43. Keith, L.B., Todd, A.W., Brand, C.J., Adamcik, R.S. & Rusch, D.H. (1977) An analysis of predation during a cyclic fluctuation of snowshoe hares. Proceedings to the International Congress of Game Biologists, 13, 151-175.
44. Keith, L.B. & Windberg, L.A. (1978) A demographic analysis of the snowshoe hare cycle. Wildlife Monographs, 58, 1-70.
45. Keymer, A.E. & Dobson, A.P. (1987) The ecology of helminths in populations of small mammals. Mammal Review, 17, 105-116.
46. Korpimaki, E. & Norrdahl, K. (1991) Numerical and functional responses of kestrels, short-eared owls and long-eared owls to vole densities. Ecology, 72, 814-826.
47. Krebs, C.J., Boutin, S., Boonstra, R., Sinclair, A.R.E., Smith, J.N.M., Dale, M.R.T., Martin, K. & Turkington, R. (1995) Impact of food and predation on the snowshoe hare cycle. Science, 269, 1112-1115.
48. Laine, K. & Henttonen, H. (1983) The role of plant production in microtine cycles in northern Fennoscandinavia. Oikos, 40, 407-418.
49. Lloyd, M. & Dybas, H.S. (1966) The periodical cicada problem: I. Population ecology. Evolution, 20, 133-149.
50. Luttich, S.N., Keith, L.B. & Stephenson, J.D. (1971) Population dynamics of the red-tailed hawk (Buteo jamaicensis) at Rochester, Alberta. Auk, 88, 75-87.
51. May, R.M. & Anderson, R.M. (1978) Regulation and stability of host-parasite population interactions. II. Destabilizing processes. Journal of Animal Ecology, 47, 249-268.
52. May, R.M. (1972) Limit cycles in predator-prey communities. Science, 177, 900-902.
53. May, R.M. (1974) Stability and Complexity in Model Ecosystems. Princeton University Press, Princeton, NJ.
54. May, R.M. (1983) Parasitic infections as regulators of animal populations. American Scientist, 71, 36-45.
55. McCallum, H. & Dobson, A. (1995) Detecting disease and parasite threats to endangered species and ecosystems. Trends in Ecology and Evolution, 10, 190-194.
56. Michel, J.F., Lancaster, M.B. & Hong, C. (1975) Arrested development of Obeliscoides cuniculi: the effect of size of innoculum. Journal of Comparative Pathology, 85, 307-315.
57. Mihok, S., Turner, B.N & Iversen, S.L. (1985) The characterization of vole population dynamics. Ecological Monographs, 55, 399-420.
58. Minchella, D.J. & Scott, M.E. (1991) Parasitism: a cryptic determinant of animal community structure. Trends in Ecology and Evolution, 6, 250-254.
59. Moss, G.D. (1971) The nature of the immune response of the mouse to the bile duct cestode, Hymenolepis microstoma. Parasitology, 62, 285-294.
60. Murray, D.L., Cary, J.R. & Keith, L.B. (1997) Interactive effects of sublethal nematodes and nutritional status on snowshoe hare vulnerability to predation. Journal of Animal Ecology, 66, 250-264.
61. Murray, D.L., Keith, L.B. & Cary, J.R. (1996) The effect of antihelminthic treatment on the parasite burden of free-ranging snowshoe hares. Canadian Journal of Zoology, 74, 1604-1611.
62. Myers, J.H. (1988) Can a general hypothesis explain population cycles of forest Lepidoptera. Advances in Ecological Research, 2, 55-66.
63. Nellis, C.H. & Keith, L.B. (1976) Population dynamics of coyotes in central Alberta, 1964-68. Journal of Wildlife Management, 40, 389-399.
64. Nellis, C.H., Whetmore, S.P. & Keith, L.B. (1972) Lynxprey interactions in central Alberta. Journal of Wildlife Management, 36, 320-329.
65. Pech, R.P., Sinclair, A.R.E., Newsome, A.E. & Catling, P.C. (1992) Limits to predator regulation of rabbits in Australia: evidence from predator-removal experiments. Oecologia, 89, 102-112. :
66. Perrin, W.F. & Powers, J.E. (1980) Role of a nematode in natural mortality of spotted dolphins. Journal of Wildlife Management, 44, 960-963.
67. Potts, G.R, Tapper, S.C. & Hudson, P.J. (1984) Population fluctuations in red grouse: analysis of bag records and a simulation model. Journal of Animal Ecology, 53, 21-36.
68. Reeve, J.D., Cronin, J.T. & Strong, D.R. (1994) Parasitism and generation cycles in a salt-marsh planthopper. Journal of Animal Ecology, 63, 912-920.
69. Royama, T. (1992) Analytical Population Dynamics. Chapman and Hall, New York.
70. Rusch, D.H., Meslow, E.C., Doerr, P.D. & Keith, L.B. (1972) Response of great horned owl populations to changing prey densities. Journal of Wildlife Management, 36, 282-296.
71. Russell, S.W., Baker, N.F. & Raizes, G.S. (1966) Experimental Obeliscoides cuniculi infections in rabbits: comparison with Trichostrongylus and Ostertagia infections in cattle and sheep. Experimental Parasitology, 19, 163-173.
72. Sinclair, A.R.E., Gosline, J.M., Holdsworth, G., Krebs, C.J., Boutin, S., Smith, J.N.M., Boonstra, R. & Dale, M. (1993) Can the solar cycle and climate synchronize the snowshoe hare cycle in Canada? Evidence from tree rings and ice cores. American Naturalist, 141, 173-198.
73. Stairs, G. (1972) Pathogenic microorganisms in the regulation of forest insect populations. Annual Review of Entomology, 17, 355-373.
74. Stout, I.J. & Cornell, G.W. (1976) Nonhunting mortality of fledged North American waterfowl. Journal of Wildlife Management, 40, 681-693.
75. Tanner, J.T. (1975) The stability and the intrinsic growth rate of prey and predator populations. Ecology, 62, 327-335.
76. Todd, A.W. & Keith, L.B. (1983) Coyote demography during a snowshoe hare decline in Alberta. Journal of Wildlife Management, 47, 394-404.
77. Todd, A.W., Keith, L.B. & Fischer, C.A. (1981) Population ecology of coyotes during a fluctuation of snowshoe hares Journal of Wildlife Management, 45, 629-640.
78. van Riper, C., van Riper, S.G., Goff, M.L. & Laird, M. (1986) The epizoology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs, 56, 327-344.
79. Wakelin, D. (1987) The role of the immune response in helminth population regulation. International Journal for Parasitology, 17, 291-297.
80. Woolf, A., Shoemaker, D.R. & Cooper, M. (1993) Evidence of tularemia regulating a semi-isolated cottontail rabbit population. Journal of Wildlife Management, 57, 144-157.
81. Yuill, T.M. (1964) Effects of gastrointestinal parasites on cottontails. Journal of Wildlife Management, 28, 20-26.
82. Yuill, T.M. (1987) Diseases as components of mammalian ecosystems: mayhem and subtlety. Canadian Journal of Zoology, 65, 1061-1066.